Genomes of ubiquitous marine and hypersaline Hydrogenovibrio, Thiomicrorhabdus and Thiomicrospira spp. encode a diversity of mechanisms to sustain chemolithoautotrophy in heterogeneous environments

Abstract

Chemolithoautotrophic bacteria from the genera Hydrogenovibrio, Thiomicrorhabdus and Thiomicrospira are common, sometimes dominant, isolates from sulfidic habitats including hydrothermal vents, soda and salt lakes and marine sediments. Their genome sequences confirm their membership in a deeply branching clade of the Gammaproteobacteria. Several adaptations to heterogeneous habitats are apparent. Their genomes include large numbers of genes for sensing and responding to their environment (EAL- and GGDEF-domain proteins and methyl-accepting chemotaxis proteins) despite their small sizes (2.1-3.1 Mbp). An array of sulfur-oxidizing complexes are encoded, likely to facilitate these organisms' use of multiple forms of reduced sulfur as electron donors. Hydrogenase genes are present in some taxa, including group 1d and 2b hydrogenases in Hydrogenovibrio marinus and H. thermophilus MA2-6, acquired via horizontal gene transfer. In addition to high-affinity cbb cytochrome c oxidase, some also encode cytochrome bd-type quinol oxidase or ba -type cytochrome c oxidase, which could facilitate growth under different oxygen tensions, or maintain redox balance. Carboxysome operons are present in most, with genes downstream encoding transporters from four evolutionarily distinct families, which may act with the carboxysomes to form CO concentrating mechanisms. These adaptations to habitat variability likely contribute to the cosmopolitan distribution of these organisms.

Genomes of Neutrophilic Sulfur-Oxidizing Chemolithoautotrophs Representing 9 Proteobacterial Species From 8 Genera

“…Phylogenetically diverse bacteria have the capability of utilizing sulfur compounds as electron donors for respiration or phototrophic carbon fixation (Muyzer et al, 2013; Sorokin et al, 2013; Dahl, 2017). These sulfur-oxidizing bacteria have sulfur oxidation pathways consisting of various components (examples are shown in Figure 1), and distribution of the genes for sulfur oxidation has been investigated in diverse prokaryotic genomes (e.g., Meyer and Kuever, 2007; Meyer et al, 2007; Gregersen et al, 2011; Watanabe et al, 2014; Scott et al, 2018). These bacteria are also involved in the carbon and nitrogen cycles, playing crucial roles in natural environments (e.g., Mattes et al, 2013; Prokopenko et al, 2013; Herrmann et al, 2015; Dyksma et al, 2016; Lau et al, 2016).…”

A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index

“…(1,420 bp, GenBank accession number DQ390450 [27] and the full-length versions of this gene (1,439 bp each; IMG identifiers [IDs] 2518265101 and 2518265550) originating from a draft genome (28) and used in this study. The phylogenetic placement of this organism also supports the idea that H. halophilus is distinctly positioned in its own clade as it branches away from the cluster of other Hydrogenovibrio spp.…”

Diversity in CO 2 -Concentrating Mechanisms among Chemolithoautotrophs from the Genera Hydrogenovibrio , Thiomicrorhabdus , and Thiomicrospira , Ubiquitous in Sulfidic Habitats Worldwide

“…The genome sequences of Thiomicrorhabdus arctica and Thiomicrorhabdus sp. strain Milos-T2 lack carboxysome loci (19); either these loci are absent or they are present in a portion of the genome that has yet to be sequenced. Genomes from all four sequenced members of Thiomicrorhabdus were scrutinized for evidence of rearrangement in the region associated with the carboxysome locus.…”

“…Several members of the genera Thiomicrospira, Thiomicrorhabdus, and Hydrogenovibrio, organisms taxonomically affiliated with H. crunogenus (18), have had their genomes sequenced. Taxa for sequencing were selected to represent both the taxonomic breadth of these genera and the range of habitats from which these organisms have been isolated, including shallow and deep-sea hydrothermal vents, coastal sediments, and soda and salt lakes (19). Despite the rather narrow taxonomic range of the organisms sequenced, the genome data suggested a surprising diversity in mechanisms for DIC uptake and fixation.…”

“…For members of Thiomicrospira, genes encoding carboxysome components are present, but genes encoding carboxysomal carbonic anhydrase are lacking. In their place, each species carries a gene without apparent homologs beyond this genus (19), raising the possibility that these genes encode a novel form of carboxysomal carbonic anhydrase. In all cases, when present, carboxysome loci are followed by genes encoding transporters from four evolutionarily distinct families.…”